Egr-1 induces DARPP-32 expression in striatal medium spiny neurons via a conserved intragenic element

Journal of Neuroscience

Volumn 32, Issue 20, 2012, Pages 6808-6818

  Keilani, Serene ^a   Chandwani, Samira ^a   Dolios, Georgia ^a   Bogush, Alexey ^b   Beck, Heike ^c   Hatzopoulos, Antonis K ^d   Rao, Gadiparthi N ^e   Thomas, Elizabeth A ^f   Wang, Rong ^a   Ehrlich, Michelle E ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^d VANDERBILT UNIVERSITY   (United States)

^e UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; EARLY GROWTH RESPONSE FACTOR 1; NUCLEAR PROTEIN; OLIGONUCLEOTIDE; PHOSPHOPROTEIN DARPP 32;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE; GENE MUTATION; IMMUNOCYTOCHEMISTRY; INTRON; MALE; MASS SPECTROMETRY; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PP1R1B GENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOUTHERN BLOTTING; SPINY NEURON; STRIATE CORTEX; WESTERN BLOTTING;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CORPUS STRIATUM; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION REGULATION; INTRONS; MICE; NERVE TISSUE PROTEINS; NEURONS; PRIMARY CELL CULTURE; PROTEIN BINDING; RATS; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

EID: 84861112814     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5448-11.2012     Document Type: Article

References (69)

1. Alder J, Thakker-Varia S, Bangasser DA, Kuroiwa M, Plummer MR, Shors TJ, Black IB (2003) Brain-derived neurotrophic factor-induced gene expression reveals novel actions of VGF in hippocampal synaptic plasticity. J Neurosci 23:10800-10808.
2. Arlotta P, Molyneaux BJ, Jabaudon D, Yoshida Y, Macklis JD (2008) Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J Neurosci 28:622-632.
3. Aubry L, Bugi A, Lefort N, Rousseau F, Peschanski M, Perrier AL (2008) Striatal progenitors derived from human ES cells mature into DARPP-32 neurons in vitro and in quinolinic acid-lesioned rats. Proc Natl Acad Sci U S A 105:16707-16712.
4. Beck H, Semisch M, Culmsee C, Plesnila N, Hatzopoulos AK (2008) Egr-1 regulates expression of the glial scar component phosphacan in astrocytes after experimental stroke. Am J Pathol 173:77-92.
5. Beckwith JR, Signer ER, Epstein W (1966) Transposition of the Lac region of E. coli. Cold Spring Harb Symp Quant Biol 31:393-401.
6. Blau S, Daly L, Fienberg A, Teitelman G, Ehrlich ME (1995) DARPP-32 promoter directs transgene expression to renal thick ascending limb of loop of Henle. Am J Physiol 269:F564-F570.
7. Bogush AI, McCarthy LE, Tian C, Olm V, Gieringer T, Ivkovic S, Ehrlich ME (2005) DARPP-32 genomic fragments drive Cre expression in postnatal striatum. Genesis 42:37-46.
8. Bogush A, Pedrini S, Pelta-Heller J, Chan T, Yang Q, Mao Z, Sluzas E, Gieringer T, Ehrlich ME (2007) AKT and CDK5/p35 mediate brain-derived neurotrophic factor induction of DARPP-32 in medium size spiny neurons in vitro. J Biol Chem 282:7352-7359.
9. Boyle KB, Hadaschik D, Virtue S, Cawthorn WP, Ridley SH, O'Rahilly S, Siddle K (2009) The transcription factors Egr1 and Egr2 have opposing influences on adipocyte differentiation. Cell Death Differ 16:782-789.
10. Brown TB, Bogush AI, Ehrlich ME (2008) Neocortical expressionof mutant huntingtin is not required for alterations in striatal gene expression or motor dysfunction in a transgenic mouse. Hum Mol Genet 17:3095-3104.
11. Caiazzo M, Dell'Anno MT, Dvoretskova E, Lazarevic D, Taverna S, Leo D, Sotnikova TD, Menegon A, Roncaglia P, Colciago G, Russo G, Carninci P, Pezzoli G, Gainetdinov RR, Gustincich S, Dityatev A, Broccoli V (2011) Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 476:224-227.
12. Calella AM, Nerlov C, Lopez RG, Sciarretta C, vonBohlenund Halbach O, Bereshchenko O, Minichiello L (2007) Neurotrophin/Trk receptor signaling mediates C/EBPalpha, -beta and NeuroD recruitment to immediate-early gene promoters inneuronal cells and requires C/EBPs to induce immediate-early gene transcription. Neural Dev 2:4.
13. Chang CW, Tsai CW, Wang HF, Tsai HC, Chen HY, Tsai TF, Takahashi H, Li HY, Fann MJ, Yang CW, Hayashizaki Y, Saito T, Liu FC (2004) Identification of a developmentally regulated striatum-enriched zinc-finger gene, Nolz-1, in the mammalian brain. Proc Natl Acad Sci USA 101:2613-2618.
14. Davis W Jr, Chen ZJ, Ile KE, Tew KD (2003) Reciprocal regulation of expression of the human adenosine 5'-triphosphate binding cassette, subfamily A, transporter 2 (ABCA2) promoter by the early growth response-1 (EGR-1) and Sp-family transcription factors. Nucleic Acids Res 31:1097-1107.
15. Decker EL, Skerka C, Zipfel PF (1998) The early growth response protein (EGR-1) regulates interleukin-2 transcription by synergistic interaction with the nuclear factor of activated T cells. J Biol Chem 273:26923-26930.
16. Desplats PA, Kass KE, Gilmartin T, Stanwood GD, Woodward EL, Head SR, Sutcliffe JG, Thomas EA (2006) Selective deficits in the expression of striatal-enriched mRNAs in Huntington's disease. J Neurochem 96:743-757.
17. Desplats PA, Lambert JR, Thomas EA (2008) Functional roles for the striatal-enriched transcription factor, Bcl11b, in the control of striatal gene expression and transcriptional dysregulation in Huntington's disease. Neurobiol Dis 31:298-308.
18. Ehrlich ME, Rosen NL, Kurihara T, Shalaby IA, Greengard P (1990) DARPP-32 development in the caudate nucleus is independent of afferent input from the substantia nigra. Brain Res Dev Brain Res 54:257-263.
19. Flames N, Hobert O (2011) Transcriptional control of the terminal fate of monoaminergic neurons. Annu RevNeurosci 34:153-184.
20. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273-W279.
21. 2+ signals evoked via the N-methyl-D-aspartate (NMDA) receptor. Brain Res 1366:18-26.
22. Gadgil H, Jurado LA, Jarrett HW (2001) DNA affinity chromatography of transcription factors. Anal Biochem 290:147-178.
23. Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 15:285-320.
24. Gerfen CR, Young WS 3rd (1988) Distribution of striatonigral and striato-pallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res 460:161-167.
25. Gokce O, Runne H, Kuhn A, Luthi-Carter R (2009) Short-term striatal gene expression responses to brain-derived neurotrophic factor are dependent on MEK and ERK activation. PLoS One 4:e5292.
26. Graybiel AM (2005) The basal ganglia: learning new tricks and loving it. Curr Opin Neurobiol 15:638-644.
27. Grebb JA, Girault JA, Ehrlich M, Greengard P (1990) Chronic treatment of rats with SCH-23390 or raclopride does not affect the concentrations of DARPP-32 or its mRNA in dopamine-innervated brain regions. J Neurochem 55:204-207.
28. Greengard P, Allen PB, Nairn AC (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23:435-447.
29. Gustafson EL, Ehrlich ME, Trivedi P, Greengard P (1992) In situ hybridization analysis of the development of DARPP-32 and ARPP-21 in rat striatum. Neuroscience 51:65-75.
30. Handen JS, Rosenberg HF (1997) An improved method for Southwestern blotting. Front Biosci 2:c9-c11.
31. Hobert O, Carrera I, Stefanakis N (2010) The molecular and gene regulatory signature of a neuron. Trends Neurosci 33:435-445.
32. Hodges A, Strand AD, Aragaki AK, Kuhn A, Sengstag T, Hughes G, Elliston LA, Hartog C, Goldstein DR, Thu D, Hollingsworth ZR, Collin F, Synek B, Holmans PA, Young AB, Wexler NS, Delorenzi M, Kooperberg C, Au-good SJ, Faull RL, Olson JM, Jones L, Luthi-Carter R (2006) Regional and cellular gene expression changes in human Huntington's disease brain. Hum Mol Genet 15:965-977.
33. Huang RP, Fan Y, Ni Z, Mercola D, Adamson ED (1997) Reciprocal modulation between Sp1 and Egr-1. J Cell Biochem 66:489-499.
34. Ivkovic S, Ehrlich ME (1999) Expression of the striatal DARPP-32/ ARPP-21 phenotype in GABAergic neurons requires neurotrophins in vivo and in vitro. J Neurosci 19:5409-5419.
35. Ivkovic S, Polonskaia O, Farinas I, Ehrlich ME (1997) Brain-derived neurotrophic factor regulates maturation of the DARPP-32 phenotype in striatal medium spiny neurons: studies in vivo and in vitro. Neuroscience 79:509-516.
36. Jain M, Armstrong RJ, Barker RA, Rosser AE (2001) Cellular and molecular aspects of striatal development. Brain Res Bull 55:533-540.
37. Jiang D, Jia Y, Zhou Y, Jarrett HW (2009) Two-dimensional southwestern blotting and characterization of transcription factors on-blot. J Proteome Res 8:3693-3701.
38. Kaiser UB, Halvorson LM, Chen MT (2000) Sp1, steroidogenic factor 1 (SF-1), and early growth response protein 1 (egr-1) binding sites form a tripartite gonadotropin-releasing hormone response element in the rat luteinizing hormone-beta gene promoter: an integral role for SF-1. Mol Endocrinol 14:1235-1245.
39. Keilani S, Sugaya K (2008) Reelin induces a radial glial phenotype in human neural progenitor cells by activation of Notch-1. BMC Dev Biol 8:69.
40. Knapska E, Kaczmarek L (2004) Gene for neuronal plasticityin the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK? Prog Neurobiol 74:183-211.
41. Kundumani-Sridharan V, Niu J, Wang D, Van Quyen D, Zhang Q, Singh NK, Subramani J, Karri S, Rao GN (2010) 15(S)-hydroxyeicosatetraenoic acid-induced angiogenesis requires Src-mediated Egr-1-dependent rapid induction of FGF-2 expression. Blood 115:2105-2116.
42. Lin JX, Leonard WJ (1997) The immediate-early gene product Egr-1 regulates the human interleukin-2 receptor beta-chain promoter through noncanonical Egr and Sp1 binding sites. Mol Cell Biol 17:3714-3722.
43. Lobo MK, Karsten SL, Gray M, Geschwind DH, Yang XW (2006) FACS-array profilingof striatal projection neuron subtypesin juvenile and adult mouse brains. Nat Neurosci 9:443-452.
44. Luthi-Carter R, Strand A, Peters NL, Solano SM, Hollingsworth ZR, Menon AS, Frey AS, Spektor BS, Penney EB, Schilling G, Ross CA, Borchelt DR, Tapscott SJ, Young AB, Cha JH, Olson JM (2000) Decreased expression of striatal signaling genesinamouse model of Huntington's disease. Hum Mol Genet 9:1259-1271.
45. Luthi-Carter R, Hanson SA, Strand AD, Bergstrom DA, Chun W, Peters NL, Woods AM, Chan EY, Kooperberg C, Krainc D, Young AB, Tapscott SJ, Olson JM (2002) Dysregulation of gene expression in the R6/2 model of polyglutamine disease: parallel changes in muscle and brain. Hum Mol Genet 11:1911-1926.
46. Minichiello L, Calella AM, Medina DL, Bonhoeffer T, Klein R, Korte M (2002) Mechanism of TrkB mediated hippocampal long-term potentia-tion. Neuron 36:121-137.
47. Minig V, Kattan Z, van Beeumen J, Brunner E, Becuwe P (2009) Identification of DDB2 protein as a transcriptional regulator of constitutive SOD2 gene expression in human breast cancer cells. J Biol Chem 284: 14165-14176.
48. Ouimet CC, Langley-Gullion KC, Greengard P (1998) Quantitative immu-nocytochemistry of DARPP-32-expressing neurons in the rat caudatopu-tamen. Brain Res 808:8-12.
49. Papanikolaou NA, Sabban EL (2000) Ability of Egr1 to activate tyrosine hydroxylase transcription in PC12 cells. Cross-talk with AP-1 factors. J Biol Chem 275:26683-26689.
50. Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20:91-127.
51. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spec-trometry data. Electrophoresis 20:3551-3567.
52. Sánchez-Danés A, Consiglio A, Richaud Y, Rodríguez-Pizà I, Dehay B, Edel M, Bové J, Memo M, Vila M, Raya A, Izpisua Belmonte JC (2012) Efficient generation of A9 midbrain dopaminergic neurons by lentiviral delivery of LMX1A in human embryonic stem cells and iPS cell. Hum Gene Ther 23:56-69.
53. Schreiber E, Matthias P, Müller MM, Schaffner W (1989) Rapid detection of octamer binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res 17:6419.
54. Searle BC (2010) Scaffold: abioinformatic tool for validating MS/MS-based proteomics studies. Proteomics 10:1265-1269.
55. Snyder-Keller A, Chandra R, Lin Y, Mitchell ES (2002) Basal EGR-1 (zif268, NGFI-A, Krox-24) expression in developing striatal patches: role of dopamine and glutamate. Brain Res 958:297-304.
56. Son EY, Ichida JK, Wainger BJ, Toma JS, Rafuse VF, Woolf CJ, Eggan K (2011) Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 9:205-218.
57. Spektor BS, Miller DW, Hollingsworth ZR, Kaneko YA, Solano SM, Johnson JM, Penney JB, Young AB, Luthi-Carter R (2002) Differential D1 and D2 receptor-mediated effects on immediate early gene induction in a transgenic mouse model of Huntington's disease. Brain Res Mol Brain Res 102:118-128.
58. Stroppolo A, Guinea B, Tian C, Sommer J, Ehrlich ME (2001) Roleofphos-phatidylinositide 3-kinase in brain-derived neurotrophic factor-induced DARPP-32 expression in medium size spiny neurons in vitro. J Neuro-chem 79:1027-1032.
59. Svenningsson P, Nishi A, Fisone G, Girault JA, Nairn AC, Greengard P (2004) DARPP-32: an integrator of neurotransmission. Annu Rev Pharmacol Toxicol 44:269-296.
60. Tai TC, Wong DL (2003) Protein kinase A and protein kinase C signaling pathway interaction in phenylethanolamine N-methyltransferase gene regulation. J Neurochem 85:816-829.
61. Tan L, Peng H, Osaki M, Choy BK, Auron PE, Sandell LJ, Goldring MB (2003) Egr-1 mediates transcriptional repression of COL2A1 promoter activity by interleukin-1beta. J Biol Chem 278:17688-17700.
62. 2+-regulated transcription factor. Cell Calcium 47:397-403.
63. Thomas EA, Coppola G, Desplats PA, Tang B, Soragni E, Burnett R, Gao F, Fitzgerald KM, Borok JF, Herman D, Geschwind DH, Gottesfeld JM (2008) The HDAC inhibitor 4b ameliorates the disease phenotype and transcriptional abnormalities in Huntington's disease transgenic mice. Proc Natl Acad Sci USA 105:15564-15569.
64. Thomas EA, Coppola G, Tang B, Kuhn A, Kim S, Geschwind DH, Brown TB, Luthi-Carter R, Ehrlich ME (2011) In vivo cell-autonomous transcriptional abnormalities revealed in mice expressing mutant huntingtin in striatal but not cortical neurons. Hum Mol Genet 20:1049-1060.
65. Valjent E, Corvol JC, Pages C, Besson MJ, Maldonado R, Caboche J (2000) Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J Neurosci 20:8701-8709.
66. Valjent E, Aubier B, Corbille AG, Brami-Cherrier K, Caboche J, Topilko P, Girault JA, Herve D (2006) Plasticity-associated gene Krox24/Zif268 is required for long-lasting behavioral effects of cocaine. J Neurosci 26:4956-4960.
67. van der Kooy D, Fishell G (1987) Neuronal birthdate underlies the development of striatal compartments. Brain Res 401:155-161.
68. Wells T, Rough K, Carter DA (2011) Transcription mapping of embryonic rat brain reveals EGR-1 induction in SOX2 neural progenitor cells. Front Mol Neurosci 4:6.
69. Zucker B, Luthi-Carter R, Kama JA, Dunah AW, Stern EA, Fox JH, Standaert DG, Young AB, Augood SJ (2005) Transcriptional dysregulation in striatal projection- and interneurons in a mouse model of Huntington's disease: neuronal selectivity and potential neuroprotective role of HAP1. Hum Mol Genet 14:179-189.